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Marine Pollution Bulletin 53 (2006) 272–286

The effect of the ‘‘Prestige’’ oil spill on the planktonof the N–NW Spanish coast

Manuel Varela a,*, Antonio Bode a, Jorge Lorenzo a, M. Teresa Alvarez-Ossorio a,Ana Miranda b, Teodoro Patrocinio b, Ricardo Anadon c, Leticia Viesca c,

Nieves Rodrıguez c, Luis Valdes d, Jesus Cabal d, Angel Urrutia d, Carlos Garcıa-Soto e,Menchu Rodrıguez e, Xose Anton Alvarez-Salgado f, Steve Groom g

a Instituto Espanol de Oceanografia, Muelle de Animas s/n, La Coruna, Spainb Instituto Espanol de Oceanografia, Cabo Estay, Vigo, Spain

c Laboratorio de Ecologıa, Universidad de Oviedo, Spaind Instituto Espanol de Oceanografia, Paseo del Arbeyal, Gijon, Spain

e Instituto Espanol de Oceanografia, Promontorio de San Martın s/n, Santander, Spainf Instituto de Investigaciones Marinas, Eduardo Cabello 6, Vigo, Spain

g Plymouth Marine Lab., Prospect Place, The Hoe, Plymouth PL1 3DH, United Kingdom

Abstract

Chlorophyll, primary production, zooplankton biomass and the species composition of phytoplankton and zooplankton were studiedin 2003, after the Prestige shipwreck. The information obtained was compared to previous data series available for the area affected bythe spill. A large data series on plankton variables for the N–NW Spanish coast existed, and therefore a realistic evaluation of the effectsby comparison with the range of natural variability could be carried out. We emphasized the evaluation of impact during the springbloom, the first important biological event after the spill. Some minor changes were observed occasionally, but they did not showany clear pattern and were more related to the natural variability of the ecosystem than to effect of the spill. Plankton community struc-ture did not undergo any changes. Only a few species were more abundant during spring 2003 than in previous years. No significantchanges were detected in the planktonic community during productive periods, such as the spring bloom and the summer blooms relatedto intrusions of East North Atlantic Central Waters. The lack of evidence of the effects of the spill on planktonic communities is dis-cussed in terms of the characteristics of the fuel, the high dynamics of the water masses, the biological mechanisms through whichthe fuel from the surface waters is transferred to the sea floor and, particularly, the influence of the natural variability by means of largeand meso-scale hydrographic processes in the area under study. At the present time it is not possible to determine any minor effects thespill may have had on the plankton owing to the great variability of the planktonic cycles and the short-term impact of the oil from thePrestige on the pelagic system.� 2005 Elsevier Ltd. All rights reserved.

Keywords: Chlorophyll; Primary production; Zooplankton; Phytoplankton; Species composition; Oil spill; Prestige oil tanker; Galicia; NW Spain

1. Introduction

Oil tanker accidents have occurred frequently along theGalician coast. Over the course of the last 30 years, there

0025-326X/$ - see front matter � 2005 Elsevier Ltd. All rights reserved.

doi:10.1016/j.marpolbul.2005.10.005

* Corresponding author. Tel.: +34 981 205362; fax: +34 981 229077.E-mail address: manuel.varela@co.ieo.es (M. Varela).

have been three major oil spills: the Urquiola in 1976, theAegean Sea in 1992 and finally the Prestige in November2002. The first two affected a localized area of the coastoff A Coruna (Fig. 1), while the last spill had a wider areaof influence, extending from northern Portugal to thesouthern French coast (Garcıa-Soto, 2004).

Over the last 30 years, numerous studies on the influenceof oil on plankton communities have been carried out. In

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Fig. 1. Map of the study area showing the sampling locations from the IEO Core Project Studies on Time Series of Oceanographic Data, and the zonecovered by Pelacus cruises from 1999 to 2003. SG: South Galicia; NG: North Galicia. WBB: West Bay of Biscay; EBB: East Bay of Biscay. Open circles:Shelf stations (around 100 m depth). Filled circles: Coastal stations (around 20 m depth). Rectangles delimit the areas where satellite information isavailable: OMEX box area (primary production), between Cape Finisterre and Vigo; and the area in front of Gijon (chlorophyll).

M. Varela et al. / Marine Pollution Bulletin 53 (2006) 272–286 273

general, three main approaches have been used: cultures ofsingle species, mesocosms with natural phytoplanktonassemblages, and studies undertaken in natural or in situconditions. The first two approaches provide a good ideaof the potential toxicity on planktonic species (Lannergren,1978; Vargo et al., 1982; Gin et al., 2001), the differentialtoxicity depending on the type of crude (Doerffer, 1992),the species-specific response (Bate and Crafford, 1985;Ostgaard et al., 1984), and the capability of plankton tometabolize hydrocarbons (Corner, 1975; Walters, 1982).However, the conclusions are often inconsistent and there-fore difficult to extrapolate to the natural environment(Spooner and Corkett, 1979; Mahoney and Haskin, 1980;Davenport, 1982). Mesocosms have also been largely usedfor the evaluation of oil spill impact (Lee et al., 1978a;Gearing et al., 1979; Thomas et al., 1981; Scholten et al.,1987; Ohwada et al., 2003). Natural assemblages can beused but there are alterations stemming from enclosure ascompared to the natural environment. Natural planktoncommunities are the final result of complex synergies orantagonisms among organisms and the influence of hydro-graphic conditions which are limited or absent in culturesand mesocosms.

Therefore, the most realistic approach seems to be thein situ study. However, a complete assessment of theeffects of the oil spill on plankton communities throughthis approach is often difficult because many factors areinvolved. The effects are largely dependent not only onthe original components of the crude (Davenport, 1982;Shailaja, 1988; Bate and Crafford, 1985; Doerffer, 1992;Gin et al., 2001), but also on the products resulting fromdegradation which can be more toxic than the originalfuel (Lacaze and Villedon de Naıde, 1976). The effect ofoil is also largely dependent on the structure of plank-tonic communities. The response of plankton to fuel isnot only species specific, with a great variability in sensi-

tivity (Thomas et al., 1981; Throndsen, 1982; Ostgaardet al., 1984), but also clone-specific (Mahoney andHaskin, 1980). The effect is also dependent on the naturalenvironmental conditions. The inhibition of growth ratecaused by oil is highly temperature-dependent (de laCruz, 1982).

In addition, relationships among organisms in the pela-gic system may conceal the possible effects of contami-nants. Some studies reported an increase in primaryproductivity, but it was not clearly demonstrated whetherthis was caused by a stimulation of photosynthesis or adecrease in zooplankton grazing caused by oil (Lanner-gren, 1978; Johansson et al., 1980).

Finally, natural variability is probably the main obstaclestanding in the way of being able to accurately determinethe effects of oil spills on planktonic organisms. The natu-ral seasonal variation in the marine ecosystems, the mobil-ity of water masses, the patchiness in spatial and temporaldistribution of planktonic organisms make it difficult tocarry out quantitative sampling and to identify the effectsof pollution (Dicks, 1982; Varela et al., 1996).

Natural variability is especially marked in the N–NWIberian Peninsula where phytoplankton blooms show greatfluctuations (Varela, 1992; Bode et al., 2002), depending onthe intensity of meso and large-scale oceanographic eventsaffecting the area such as the Iberian Poleward Currentduring spring (Frouin et al., 1990; Alvarez-Salgado et al.,2003), and coastal upwelling of Eastern North AtlanticCentral Waters (ENACW) during the summer (Fraga,1981; Blanton et al., 1984, 1987; Alvarez-Salgado et al.,1993). The spatial and temporal variability of the marineecosystem under study strongly limits our ability to differ-entiate the anthropogenic effects from those that occur nat-urally. A good knowledge of the range of the naturalvariability of plankton is therefore essential for a correctevaluation of the impact caused by oil.

274 M. Varela et al. / Marine Pollution Bulletin 53 (2006) 272–286

The natural variability is related to the season of year.The effects would be lessened if the spill were to occur dur-ing the winter in temperate latitudes when plankton bio-mass is comparatively low. However, spills occurringduring the spring phytoplankton bloom or summer upwell-ing blooms in N–NW Spain would produce a more seriousimpact on plankton and, as a result, on the pelagic foodweb. Therefore, the study of the effect of oil spills mustinclude an appropriate temporal scope to cover the mostimportant biological periods defined for the N–NW Span-ish coast, such as the spring bloom and the summer bloomsrelated to the upwelling of ENACW (Campos and Marino,1984; Varela, 1992; Bode et al., 1996; Casas et al., 1997,1999; Varela et al., 2001).

It should be pointed out that one of major limitationsfor the in situ evaluation of the impact of oil on the marineecosystem is the lack of adequate monitoring carried outbefore a spill as well as the inadequate or insufficient histor-ical data for consistent assessment. In 1989 the SpanishInstitute of Oceanography (IEO) implemented the researchcore project Studies on Time Series of Oceanographic Data,the backbone and objectives of which, as well as the spatialand temporal coverage, is detailed in Valdes et al. (2002).The broad data set obtained over the last few years, hasallowed for the precise quantification of the effects causedby the Prestige oil spill-in the form of relevant informationwith the appropriate temporal and spatial coverage-, on thevariability of the natural ecosystem in the affected area.

The objective of this paper is to determine whether thePrestige oil spill has affected the planktonic communitiesin the North-Western shelf of the Iberian Peninsula. Theinformation obtained after the accident, up to the year2003, was compared with the historical data available forthe purpose of answering the following questions: Havethere been any changes in plankton biomass? Has the pri-mary production changed? Have we observed any changesin the main taxonomic groups? Has there been a shift in thedominance of the characteristic plankton species? Eventhough we have made a comparison for all of 2003 cover-ing the main oceanographic periods described for the area,a major effort was dedicated to investigating the effects onthe planktonic spring bloom. The spring bloom was thefirst important production period occurring on an annualscale just after the accident and the effects of the oil spillon plankton, if any, would be first observed during thisevent. The spring bloom coincides with the spawning ofmany species of great commercial interest (mainly sardine,anchovy and mussel), so that any catastrophic impact onthe first links of the pelagic food web would result in failedor reduced recruitment.

2. Material and methods

The area of study extended from Northern Portugal toSantander, in the Southern Bay of Biscay (Fig. 1). Thelocalities of Vigo, A Coruna, Cudillero, Gijon and Santan-der were selected because reference data were available for

phytoplankton, zooplankton or both. At these locations,there are coastal laboratories belonging to the SpanishInstitute of Oceanography (IEO) integrated into the frame-work of the Core project Studies on Time Series of Ocean-

ographic Data. Standard transects of several stations weresampled monthly. Two types of stations were selected: acoastal station around 30 m depth and a shelf station atapproximately 100 m depth. In some cases and for somevariables there is information available for only one sta-tion. This is the case of phytoplankton taxonomy in A Cor-una and Cudillero, and primary production in Cudillero(Fig. 1). The sampling of plankton and the analytical pro-cedures of different variables were carried out following therecommendations of JGOFS protocols (Unesco, 1994).The methods are described in detail in several papers takenfrom studies carried out on the Galician and Cantabriancoasts (Fernandez et al., 1991; Varela, 1996; Casas et al.,1997, 1999; Bode and Varela, 1998; Varela et al., 2001; Var-ela and Prego, 2003). Chlorophyll-a (Chl-a) concentrationswere measured by fluorimetry, using acetone extracts afterfiltration through Whatman GF/F filters (Unesco, 1994).Primary production was estimated by the C-14 method,using 2 h simulated in situ conditions as described in Bodeet al. (1994). Samples for microscopic examination werepreserved in Lugol�s solution and kept cool and dark untilthey were ready to be examined following Utermohl�s tech-nique. Only two main phytoplankton groups—dinoflagel-lates and diatoms—were considered for this study.Mesozooplankton samples were collected by vertical haulswith a 200 lm mesh size Bongo net. Processing of samplesfor the estimation of biomass (dry weight), counting andidentification of species are detailed in Bode et al. (2003).

Additional information available from opportunisticcruises conducted on the shelves of the Galician and South-ern Bay of Biscay, covering the area affected by the Prestige

oil spill, was also used. Pelacus cruises are core surveys ofthe IEO which have been carried out every spring since1987. The main objective of these cruises is the acousticdetermination of biomass stock and the distribution ofpelagic fisheries. Since 1999, plankton studies have beenimplemented into the cruises in the framework of severalEU research projects (Pelasses, Sardyn). During the Pela-

cus cruises chlorophyll-a was measured as explained abovefor other areas. Phytoplankton samples were obtainedusing 20 lm mesh Bongo nets and vertical hauls from100 m depth to the surface. As in the other areas of study,only dinoflagellates and diatoms were included in the studyof the impact of oil. The wide spatial coverage of the areaaffected by the Prestige accident and the fact that the sur-vey periods coincided with the season of spring bloom havemade this information invaluable to the aim of the presentstudy.

Sea WiFS-derived chlorophyll concentrations for theperiod 1998–2003, were calculated along the IEO standardsection near Gijon (Fig. 1) at 5.29�W for shelf (43.25�N to43.69�N) and oceanic waters (44.03�N to 44.56�N). Thetemporal resolution was 8 days with a spatial resolution

M. Varela et al. / Marine Pollution Bulletin 53 (2006) 272–286 275

of 9 km. Sea WiFS-derived primary production rates werecalculated for shelf (depth < 200 m) and oceanic adjacentwaters of the OMEX Box area (41�30 0N to 43�00 0N and9�00 0W to 10�30 0W), between Cape Finisterre and Ria deVigo (Fig. 1). Composite data with 9 km resolution wereobtained from the Goddard GES distributed ActiveArchive Centre at daily, 8-day and monthly resolutions.Estimates of primary production, using satellite data asinputs, were computed following essentially the samemethod as in Joint et al. (2002). The available data coverthe period between 1998 and 2004.

The evaluation of the effects was carried out comparingthe values of the above-mentioned variables for eachmonth of the year 2003, after the Prestige accident, withmean values of these variables for the same months in pre-vious years.

3. Results

3.1. Chlorophyll and primary production

Data series chlorophyll in the stations off A Corunashowed a great year-to-year variability for the period1989–2002 as deduced from large standard deviations(Fig. 2). Higher values (mean concentrations of around100 mg Chl-a m�2 with maximum values of more than200 mg Chl-a m�2 ) were measured during spring and sum-mer, the latter related to intrusions of ENACW. The samelarge variability was observed in the data from Cudillero

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Fig. 2. Monthly integrated chlorophyll and primary production during 2003 cCoruna. Asterisk denotes significant differences (p P 0.5).

for the 1992–2002 period. However, a clear variabilitybetween zones was observed. In Cudillero, higher valueswere recorded in spring. However, chlorophyll concentra-tions in summer were significantly lower (mean and maxi-mum values of 35 and 60 mg Chl-a m�2 respectively), dueto reduced upwelling intensity as compared to Galicianwaters (Fig. 3). Similar results were observed for primaryproduction.

The water column integrated Chl-a for the differentzones in Galicia and the Bay of Biscay sampled during Pel-

acus cruises is shown in Fig. 4. Data for the 2000–2002 per-iod exhibited a great inter-annual variability. The NorthernGalician and Western Bay of Biscay consistently showedhigher values of chlorophyll in all cruises as compared toSouthern Galicia and the Eastern Bay of Biscay. Slightlylower values were found in all zones in spring 2003 withrespect to values from previous years.

SeaWiFS chlorophyll derived data for the area nearGijon (Fig. 1) showed a clear inter-annual and intra-annualvariability for both shelf and ocean waters. Chl-a concen-trations were around 0.4 mg m�3 and 0.7 mg m�3 for theocean and shelf respectively. Ocean waters showed highervalues in 1999, while shelf waters exhibited large concentra-tions in 2002. Both maxima are associated with greater var-iability as indicated by standard deviations of the data(Fig. 4). The derived primary production estimated forthe OMEX box area from satellite data (Fig. 4) showed aslight year-to-year variation. Maximum production rateswere observed for the shelf in 2001 and for oceanic waters

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Fig. 3. Monthly integrated chlorophyll and primary production during 2003 compared to pre-spill data in coastal and shelf stations in the coast offCudillero.

276 M. Varela et al. / Marine Pollution Bulletin 53 (2006) 272–286

in 1999. Minimum values for both zones were recorded in2004. Mean values of primary production were around200 gC m�2 y and 350 g cm�2 y for ocean and shelf watersrespectively. In general, satellite data showed less variabil-ity than field data, as the satellite is not able to detect thelarge vertical variations that tend to occur in the watercolumn.

3.2. Phytoplankton community

Diatoms formed the bulk of the phytoplankton commu-nity in both Galicia (A Coruna) and the Southern Bay ofBiscay (Cudillero, Asturias). Both diatoms and dinoflagel-lates exhibited large inter-annual and spatial variations aswell. Dinoflagellates presented similar values in both zoneseven though they were comparatively more abundant insummer in Cudillero (Fig. 5). Diatoms showed similarabundances in both areas during spring, but in Galicia,higher concentrations were maintained throughout thesummer until autumn. After spring, in contrast, valuesdropped significantly during summer in the Southern Bayof Biscay.

In both areas a great year-to-year variability wasobserved, especially for the more productive periods. Meandiatom values may reach 25000 · 106 cells m�2, but maxi-mum values can be up to four times higher. This high var-iability is related to the intensity of ENACW upwellingevents during the summer in Galician waters (Camposand Marino, 1984; Bode et al., 1994; Casas et al., 1997,

1999), and to meteorological and oceanographic conditions(influence of the Poleward current) prevailing duringspring, which may or may not favour the development ofa spring bloom (Casas et al., 1997; Fernandez et al.,1991; Alvarez-Salgado et al., 2003).

During the spring bloom, diatoms dominated the phyto-plankton community far above the others (Table 1). Chae-

toceros socialis was the most abundant species in the studyarea with Detonula pumila, Guinardia delicatula, Pseudo-

nitzschia cf. pungens and Skeletonema costatum as the mainaccompanying species. In contrast, dinoflagellates exhib-ited significantly lower abundances. As the standard devia-tions in Table 1 clearly show, the variations in abundanceof all the species throughout the period covered by the dataseries are extremely high.

During the Pelacus cruises, diatoms clearly dominatedthe phytoplankton community for all areas and years(Table 2). Detonula pumila, Pseudo-nitzschia cf pungens,Cerataulina pelagica and Guinardia delicatula were the mostrepresentative species. Only occasionally did some speciesof large dinoflagellates, mainly Ceratium furca, appear inremarkable quantities.

3.3. Zooplankton biomass and community

Zooplankton biomass showed a clear inshore–offshoregradient with higher values inshore (Figs. 6–8). Biomassin the coastal stations showed similar values for all thelocations (mean values of about 50 mg DW m�3 for the

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Fig. 4. Variation of integrated chlorophyll for 2003 compared to previousdata series, in different areas of N–NW Spanish coast during Pelacus

cruises. Data from. SG: South Galicia; NG: North Galicia. WBB: WestBay of Biscay; EBB: East Bay of Biscay. Yearly chlorophyll estimatesfrom SeaWiFS for the area near Gijon from 1998 to 2003. Yearly primaryproduction estimated from satellite images for the OMEX box areabetween Cape Finisterre and Ria de Vigo from 1998 to 2004.

M. Varela et al. / Marine Pollution Bulletin 53 (2006) 272–286 277

more productive periods) except for Santander where val-ues were lower (around 20 mg DW m�3 for the same peri-ods, Fig. 8). In the shelf stations, a clear spatial gradientfrom Galicia to the Southern Bay of Biscay was observed.The highest biomass values were found on the shelf offVigo in summer (between 50 and 60 mg DW m�3), andthe lowest in Santander (less than 20 mg DW m�3 in thesame period). This is related to the influence of the upwell-ing of ENACW, which is more intense in Galician waters,especially off the Rias Bajas (Fraga, 1981).

The year-to-year variability of zooplankton data islower than that of phytoplankton except for the shelf sta-tion in Vigo, where this variability is very high, especiallyin late spring and summer. This is probably related tointer-annual differences in upwelling intensity.

Calanoid copepods were by far the dominant species inthe zooplankton community in these locations and theabundance of this group showed a similar pattern to thatof biomass. The most representative calanoid species wereAcartia clausii, Calanus helgolandicus, Centropages chier-

chiae, Temora longicornis and Paracalanus parvus (Table 3).

4. Discussion

4.1. Spatial and temporal coverage

This is probably one of the most complete studies car-ried out in the sea on the effects of oil spills on planktoncommunities owing to both the wide-ranging spatial andtemporal coverage. Other complete studies (Johanssonet al., 1980) did not extend beyond two months after thespill. This greatly limits the ability to evaluate possiblechanges in the trophic structure of pelagic system depend-ing on the planktonic cycles in the area. In our case, wecontinued sampling one year after the spill to detect anypossible effects of the spill on the main biological eventsin our area: the spring bloom and the summer bloomsrelated to the upwelling of ENACW.

Most studies deal with a single or a few planktonic vari-ables, mainly the abundance of a planktonic group or chlo-rophyll (Spooner, 1977; Scholten et al., 1987; Shailaja,1988; Al-Yamani et al., 1993; Price et al., 1993; Al-Omranand Rao, 1999; Banks, 2003). In our case, however, wehave included an important set of planktonic variables(zooplankton abundance and biomass, primary produc-tion, chlorophyll, phytoplankton and zooplankton speciescomposition) to evaluate the effects from a broad perspec-tive and for differential evaluation. Finally, this study ben-efits from the availability of a large set of historicalreference data. Only a few studies have included such a vastamount of reference data and usually for only one variable(Reid, 1986; Batten et al., 1998; Banks, 2003). The lack ofinformation on the spatial and temporal variability of theecosystem is the main handicap for the natural approachof this kind of research when studying anthropogenicimpacts (Dicks, 1982; Reid, 1986; Batten et al., 1998;Banks, 2003).

4.2. The effects on plankton

A few significant statistical differences (ANOVA posthoc tests p 6 0.5) were found (Figs. 2–8). However, thesedifferences do not follow a clear temporal pattern. In someareas these differences were found during the first monthsof 2003, while in others they appeared in summer and evenin the winter immediately following the accident (Figs. 2,5–8). This suggests that differences are more likely the

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Fig. 5. Monthly integrated abundances of dinoflagellates and diatoms during 2003 compared to historical series in a shelf station on the coast off ACoruna and Cudillero. Asterisk denotes significant differences (p P 0.5).

278 M. Varela et al. / Marine Pollution Bulletin 53 (2006) 272–286

result of the natural variability of the ecosystem rather thanthe direct effect of the fuel from the Prestige.

All the significant changes observed in phytoplanktonand zooplankton species and zooplankton biomassinvolved increases in the values of these variables. Thisincrease was usually observed between 4 and 8 monthsafter the spill (Figs. 5–8). It is difficult to assume that thefuel had an effect after such a long time and that this effectwas positive, as it consistently resulted in increased biomassor abundance. Even though a detailed analysis of the rea-sons for these increased values is beyond the scope of thispaper, the peculiar hydrographic characteristics duringthe spring and summer of 2003 in the area studied, wouldprovide a more consistent explanation than those related tothe influence of the fuel (Ruiz-Villareal et al., this issue).

The spring bloom was the most important biologicalevent occurring after the oil spill. The study of the effectsduring this period is relevant as the recruitment of manyimportant shellfish and pelagic fishes depends on the nor-mal development of this bloom. During the spring bloomno significant differences in phytoplankton biomass andprimary production rates were detected. Nor were anychanges in the dominance of the main phytoplanktongroups observed. As expected for this time of the year, dia-toms formed the bulk of the phytoplankton. No significantdifferences were found for either diatoms or dinoflagellates

as compared with values reported before the spill. Similarresults were found when a comparison was made at thespecies level. Only four species accounting for only 3% ofthe total species reported in the area during this periodshowed significantly higher values after the spill (Table1). However, on the basis of these few changes, it is notpossible to conclude that these differences are a conse-quence of the accident rather than a result of natural eco-system variability, since most of the characteristic speciesof the spring phytoplankton bloom did not show statisti-cally significant differences in abundance after the spill.

A data analysis of the whole N–NW Iberian Peninsula(Pelacus Cruises) did not reveal any significant differencesbetween the 2000 and 2002 period and the year 2003. Val-ues of Chl-a were low in all the areas during 2003 but fellwithin the variability range expected in this ecosystem(Fig. 4). The dominant phytoplankton species in the differ-ent study areas during 2000–2002 matched up well withthose found in 2003 (Table 3). As expected, there was somevariability among years, but most of the characteristic spe-cies were found again after the accident throughout thearea of study. Similar results were obtained as regardsthe abundance of sardine eggs and larva (Porteiro, pers.commun.).

The available satellite information for chlorophyll andprimary production, confirms the results obtained by field-

Table 1Mean (cells/mL) and standard deviation of the more frequent phytoplankton species in a station off A Coruna and Cudillero, before and after the accidentduring the spring bloom period (February to May for A Coruna; April and May for Cudillero)

A Coruna Before (1990–2002) After (2003)

Groups and species %n Mean sd %n Mean sd

DinoflagellatesHeterocapsa niei 39 2.0 3.9 75 0.9 0.6Gyrodinium glaucum 22 0.1 0.2 75 0.4 0.3Prorocentrum balticum 33 1.3 5.2 50 4.9 8.4Scrippsiella trochoidea 24 0.5 2.1 25 0.1 0.1Torodinium roubustum 33 0.2 0.3 50 0.3 0.3

DiatomsAsterionellopsis glacialis 33 1.7 4.5 25 0.2 0.3Chaetoceros affinis 24 2.3 8.2 75 1.4 1.4Chaetoceros compressus 16 12.9 70.5 25 0.9 1.5Chaetoceros curvisetus 14 15.7 104.0 20 0.1 0.2Chaetoceros didymus 29 5.1 15.8 50 0.9 1.4Chaetoceros socialis 65 377.5 1138.1 75 31.6 44.0Chaetoceros spp 47 4.3 14.2 75 16.5 21.0Detonula pumila 43 13.3 26.3 20 0.1 0.1Guinardia delicatula 51 13.7 52.3 100 2.9 2.0Guinardia striata 14 0.3 1.6 25 0.5 0.9Lauderia borealis 20 5.6 18.8 25 0.1 0.2Leptocylindrus danicus* 51 19.7 59.9 75 151.6 258.5Leptocylindrus minimus 12 0.6 1.8 25 1.6 2.7Nitzschia sp 14 1.5 4.9 50 0.7 0.9Nitzschia longissima 51 1.3 2.5 75 2.0 2.2Pseudo-nitzschia pungens 57 12.7 28.1 75 6.3 9.5Pseudonitzschia delicatissima 10 0.6 2.5 50 0.8 1.2Skeletonema costatum 39 13.8 46.2 25 0.1 0.1Thalassionema nitzschoides 35 1.2 3.7 75 1.7 1.2Thalassiosira fallax 22 0.9 2.8 50 1.1 1.6

Other phytoplanktersPhaeocistis pouchetii 33 3.0 7.3 25 1.8 3.1Solenicola setigera 22 9.4 46.9 75 10.6 17.6

Cudillero Before (1995–2002) After (2003)

Groups and species %n Mean sd %n Mean sd

DinoflagellatesHeterocapsa niei 29 0.4 0.9 25 0.1 0.1Prorocentrum balticum* 14 0.1 0.4 100 3.2 2.6Scrippsiella trochoidea 57 0.6 0.8 50 0.2 0.2

DiatomsAsterionellopsis glacialis 14 0.2 0.7 50 0.2 0.2Bacteriastrum hyalinum 14 1.3 3.3 25 0.1 0.1Cerataulina pelagica 21 0.3 1.1 25 0.1 0.2Chaetoceros curvisetus* 14 0.2 0.6 50 16.5 16.5Chaetoceros danicus 29 0.4 0.9 25 0.1 0.1Chaetoceros socialis 7 121.4 437.7 50 191.0 191.0Detonula pumila 57 11.6 26.7 50 0.1 0.1Guinardia delicatula 57 38.3 109.2 25 0.1 0.1Leptocylindrus danicus 71 67.0 224.8 100 46.1 43.6Leptocylindrus minimus 7 0.1 0.3 50 24.6 24.6Pseudo-nitzschia pungens* 93 3.1 5.3 100 93.2 93.1Rhizosolenia setigera 36 0.4 1.1 25 0.1 0.1Skeletonema costatum 14 23.9 86.0 50 12.4 12.4

n (before): percentage of species appearance for the total number of samples (49). n (after) the same for four samples. Asterisk denotes significantdifferences (p P 0.5).

M. Varela et al. / Marine Pollution Bulletin 53 (2006) 272–286 279

work. No significant differences were observed for 2003and 2004 as compared to the previous years (Fig. 4). Dur-ing 2003 only one single bloom extended from the coast tothe oceanic Bay of Biscay near Gijon as opposed to two

blooms in the mean distribution (1998–2002). However,the inter-annual standard deviation of the second bloomis comparable to the mean so its absence in 2003 maybe considered as included in the natural year-to-year

Table 2Main phytoplankton species ranked by order of relative abundance during the 2000–2002 period before the accident and for year 2003, after the accidentfrom Pelacus Cruises

Zone Year before Year after

2000 2001 2002 2003

SG Leptocylindrus danicus Skeletonema costatum Asterionellopsis glacialis Ceratium furca

Pseudo-nitzschia cf pungens Detonula pumila Thalassiosira rotula Detonula pumila

Guinardia delicatula Ceratium furca Chaetoceros decipiens

Detonula pumila

NG Chaetoceros socialis Bacteriastrum delicatulum Thalassiosira rotula Guinardia delicatula

Pseudo-nitzschia cf pungens Skeletonema costatum Detonula pumila Detonula pumila

Guinardia delicatula Detonula pumila Thalassionema nitzschioides Chaetoceros curvisetus

Guinardia flaccida Chaetoceros curvisetus Chaetoceros decipiens

Thalassionema nitzschioides

WBB Guinardia delicatula Guinardia flaccida Detonula pumila Pseudo-nitzschia cf pungens

Detonula pumila Detonula pumila Asterionellopsis glacialis Proboscia alata

Pseudo-nitzschia cf pungens Cerataulina pelagica Ceratium furca Ceratium furca

Cerataulina pelagica Detonula pumila

Pseudo-nitzschia cf pungens

Thalassionema nitzschioides

EBB Guinardia delicatula Cerataulina pelagica Detonula pumila Pseudo-nitzschia cf pungens

Pseudo-nitzschia cf pungens Detonula pumila Ceratium furca Proboscia alata

Ceratium furca Pseudo-nitzschia cf pungens Leptocylindrus danicus

Leptocylindrus danicus Cerataulina pelagica Detonula pumila

Pseudo-nitzschia cf pungens

SG: Southern Galicia; NG: Northern Galicia; WBB: Western Bay of Biscay; EBB: Eastern Bay of Biscay. Names in lightface print: diatoms; names inboldface print: dinoflagellates.

Vigo Zooplankton Coastal station

0

30

60

90

120

150

JA FB MR AP MY JN JL AG SP OC NO DC

mg

DW

m-3

m

g D

W m

-3

mg

DW

m-3

m

g D

W m

-3

1994-20022003

*

*

Vigo Zooplankton Shelf station

0

30

60

90

120

150

JA FB MR AP MY JN JL AG SP OC NO DC

1994-20022003

* *

A Coruña Zooplankton Coastal station

0

30

60

90

120

150

JA FB MR AP MY JN JL AG SP OC NO DC

1990-20022003

*

A Coruña Zooplankton Shelf station

0

30

60

90

120

150

JA FB MR AP MY JN JL AG SP OC NO DC

1990-20022003

*

Fig. 6. Monthly variation of zooplankton biomass during 2003 compared to historical series in coastal and shelf stations on the coast off Vigo and ACoruna. Asterisk denotes significant differences (p P 0.5).

280 M. Varela et al. / Marine Pollution Bulletin 53 (2006) 272–286

Cudillero Zooplankton Shelf station

0

25

50

75

100

JA FB MR AP MY JN JL AG SP OC NO DC

1993-2002

2003

Cudillero Zooplankton Coastal station

0

25

50

75

100

JA FB MR AP MY JN JL AG SP OC NO DC

mg

DW

m-3

m

g D

W m

-3

1993-2002

2003 *

*

Fig. 7. Monthly variation of zooplankton biomass during 2003 comparedto historical series in coastal and shelf stations on the coast off Cudillero.Asterisk denotes significant differences (p P 0.5).

M. Varela et al. / Marine Pollution Bulletin 53 (2006) 272–286 281

variability of this ecosystem. Values of satellite derived pri-mary production showed no differences in 2003 as com-pared to previous years in the OMEX Box area in front

Gijón Zooplankton Coastal station

0

20

40

60

80

100

120

JA FB MR AP MY JN JL AG SP OC NO DC

mg

DW

m-3

m

g D

W m

-3

2001-20022003

Gijón Zooplankton Shelf station

0

20

40

60

80

100

120

JA FB MR AP MY JN JL AG SP OC NO DC

2001-20022003

Fig. 8. Monthly variation of zooplankton biomass during 2003 compared toSantander. Asterisk denotes significant differences (p P 0.5).

of the Rias Bajas (Fig. 4). Since most of yearly primaryproduction occurs during the spring and summer upwellingblooms, it may be concluded that these events were similarin intensity from 1998 to 2004.

The data on zooplankton do not reveal any significantshifts in biomass after the spill during the spring bloom.As in previous years, calanoid copepods were the dominantgroup of zooplankton in 2003. Statistical tests for the maincalanoid copepods during this period did not exhibit anychanges in abundance except for one species in the Riade Vigo (Table 3). As in the case of phytoplankton species,this is probably related to natural variability. Similarresults were obtained when other holoplanktonic (clado-cera, tintinids) or meroplanktonic (crustacea, briozoa orequinoderm larva) groups were considered.

4.3. Comparison with other studies

A comparison with other spills is difficult because eachone has its own characteristics with various types of oils,environmental conditions and planktonic communitiesinvolved. Despite these limitations, our results were similarto those reported in other studies. In fact, the investigationscarried out on different spills have not been able to demon-strate important effects on pelagic organisms (Michael,1977; Sandborn, 1977; Spooner, 1977). It was not possibleto demonstrate any major effects on the phytoplanktoncommunity after the Torrey Canyon (Nelson-Smith,1970), the Santa Barbara (Straughan, 1972), the Argo Mer-

chant (Kuhnhold, 1978), the Tsesis (Linden et al., 1979;Johansson et al., 1980) or the Aegean Sea (Varela et al.,

mg

DW

m-3

Santander Zooplankton Coastal station

0

20

40

60

80

100

120

JA FB MR AP MY JN JL AG SP OC NO DC

mg

DW

m-3

1991-20022003 *

Santander Zooplankton Shelf station

0

20

40

60

80

100

120

JA FB MR AP MY JN JL AG SP OC NO DC

1991-20022003

*

historical series in coastal and shelf stations on the coast off Gijon and

Table 3Mean (abundance/m3) and standard deviation of selected copepods species during the spring bloom in different areas before and after Prestige oil spill

Vigo Coruna Cudillero Santander

Before After Before After Before After Before After

Coastal stationsAcartia clausi 1572 ± 1365 695 ± 120 2630 ± 2248 4054 ± 1555Calanus helgolandicus 143 ± 111 125 ± 192 61 ± 159 253 ± 10Centropages chierchiae 73 ± 100 12 ± 15 35 ± 87 127 ± 27Paracalanus parvus 193 ± 144 641 ± 75* 341 ± 307 111 ± 42Temora longicornis 236 ± 185 206 ± 102 366 ± 461 133 ± 38 52 ± 87 14 ± 23

Shelf stationsAcartia clausi 2363 ± 5159 290 ± 32 724 ± 635 390 ± 131 200 ± 236 362 ± 293Calanus helgolandicus 2086 ± 5868 136 ± 30 25 ± 24 10 ± 8 95 ± 159 69 ± 117Centropages chierchiae 53 ± 71 18 ± 19 62 ± 83 32 ± 14 15 ± 62 17 ± 24Paracalanus parvus 478 ± 1113 161 ± 78 458 ± 443 127 ± 35 277 ± 255 279 ± 161Temora longicornis 158 ± 193 11 ± 15 87 ± 102 19 ± 13 7 ± 10 4 ± 7 28 ± 45 6 ± 7

Asterisk denotes statistical significant differences (p 6 0.5).

282 M. Varela et al. / Marine Pollution Bulletin 53 (2006) 272–286

1996). One of the drawbacks of most of the above studies isthe short duration of the research after the spill and thelack of previous information for comparisons. However,our results are comparable with those reported by Reid(1986) in the area of North Sea oil platforms or Battenet al. (1998) after the Empress oil spill, using long dataseries.

4.4. The reasons for reduced or no effects

The main question arising from the results obtained is:why were clear effects not observed in spite of the largeamount of fuel released into the pelagic system? Severalreasons can be pointed out. The first is related to the typeof fuel. The solubility of this fuel was very low so measure-ments of the water-soluble fraction indicated hydrocarbonconcentrations slightly over the background values (Gon-zalez et al., this issue). In addition, the Prestige oil was ahigh-density fuel with an elevated tendency to sink (Ser-rano et al., this issue).

The high dynamics of water in the area of the accidentfavoured not only the dispersion of oil and the eventualdecrease in the effects on plankton, but also the recoveryof the potential losses. Some papers (Spooner, 1977)reported a quick improvement in the water quality, relatedto the mixing of water masses carrying new plankton formsfrom unaltered areas.

The season of the year may also be considered an impor-tant factor to take into account when explaining the lack ofrelevant effects. The Prestige spill occurred during the win-ter when plankton biomass is low, therefore resulting inlimited effects. Extremely adverse weather conditions suchas those prevailing at the time of the accident helped tospread the fuel and clean the water column.

The low concentrations of hydrocarbons in the waterand consequently, their reduced effects may be related tothe active role of bacteria in the degradation processes ofoil. Under optimal conditions bacteria can degrade up to60–80% of crude oil (Gutnick and Rosenberg, 1977). Nohistorical data on bacteria were available in the area

affected by the Prestige spill. However, the rates of bacte-rial production measured in December and January 2003off A Coruna were slightly higher than the values measuredfor the area in previous years (Valencia et al., 2003), indi-cating the presence of oil and the importance of thesemicroorganisms in the degradation processes and the lowhydrocarbon concentrations measured (Gonzalez et al.,this issue). The presence of hydrocarbons in shelf watersoff A Coruna was confirmed by the recovery of haul netswith fuel particles and the observation of fuel adhered tothe bodies of copepods.

Several studies carried out over the last few years havedemonstrated the existence of an important mechanisminvolving oil sedimentation on the sea floor by means ofplanktonic organisms. Zooplankton is able to feed on oilparticles (Johansson et al., 1980; Sleeter and Butler,1982), which are incorporated to faecal pellets. The highsinking rates of pellets could accelerate sedimentation,especially at low water temperatures (Honjo and Roman,1978). Up to 30% of surface hydrocarbons could beremoved from surface waters through zooplankton pellets(Sleeter and Butler, 1982). This mechanism might haveoperated after the Prestige spill. Oil was frequentlyobserved in the gut contents of copepods in a station offA Coruna in December and January 2003. Previous studieson the vertical flux of organic matter showed a significantamount of zooplankton faecal pellets recovered in sedimentmoored off A Coruna (Bode et al., 1998), supporting theidea of the important role of zooplankton in the short-termremoval of fuel particle residues from surface waters. Thepossible accumulation of toxic hydrocarbons by phyto-plankton and eventual predation of zooplankton as aremoval mechanism must be taken into account as well.In any case, this process might only be important in thecase of microzooplankton (Bode et al., 2003).

The vertical transport of a large soluble fraction of oil tothe bottom may take place after adsorption to suspendedamorphous matter (detritus) and living diatoms (Ohwadaet al., 2003). Both diatoms and detritus (as well as zoo-plankton pellets), represent an important part of the mate-

M. Varela et al. / Marine Pollution Bulletin 53 (2006) 272–286 283

rial recovered in sediment traps in Galician coastal waters(Bode et al., 1998; Varela et al., 2004) and diatoms are thedominant phytoplankton group in the area (Varela et al.,2001). This would suggest a potentially important flux ofthe soluble fraction to the bottom by means of diatomsand detritus in Galician waters. The joint action of zoo-plankton diatoms and detritus could explain the high per-centage of oil transported to the bottom in the daysimmediately following a spill, ranging between 15% and39% as reported in some studies (Lee et al., 1978b; Gearinget al., 1979; Johansson et al., 1980).

The reduced impact on the pelagic system is also theresult of the capability of both phytoplankton and zoo-plankton to metabolize hydrocarbons (Walters, 1982).Many studies have demonstrated limited effects and fastrecovery of growth rates after a short lag period followingexposition to fuel, even at concentrations of one order ofmagnitude higher than those reported for the Prestige spill(Herbert and Poulet, 1980; Thomas et al., 1981). This abil-ity of the plankton would result in an additional decrease inthe concentration of hydrocarbons in the water.

The available information points to the efficiency ofphysico-chemical, physiological, and biological mecha-nisms in particular, in the dispersion or removal of petro-leum components from ocean waters and their transportto the sea bottom. These processes could explain thereduced effect on the planktonic system and the moreimportant effects on bottom communities as reported inother studies on spills (Davies et al., 1981; Lopez-Jamaret al., 1996; Varela et al., 1996).

4.5. The importance of natural variability

Some authors reported variations in planktonic systemsafter spills in some areas, but according to historical data,the magnitude of these changes were within the range ofecosystem variability. Price et al. (1993) pointed out thatthe decrease in the abundance of some larvae in the Ara-bian Gulf was more related to natural environmentalchanges than to the enormous spill resulting from the GulfWar. The minor shift in species composition observed afterthe Empress oil spill (Batten et al., 1998) may be attributedto other factors related to the natural variability of the eco-system rather than to the oil spill. Banks (2003) showedthat the variance observed in phytoplankton biomass fol-lowing the Jessica oil spill in the Galapagos Islands wasnot significant in comparison to the normally high variabil-ity between years caused by variations in the intensity of ElNino. The minor changes observed in the planktonic com-munity off A Coruna after the accident of the Aegean Sea

in 1992 were due more to the marked variability of the eco-system in the near shelf, associated to the upwelling ofENACW, than to the oil spill (Varela et al., 1996).

A good knowledge of the year-to-year variability of theecosystems affected by oil spills is essential to be able toevaluate the impact on the environment. Otherwise it willnot be possible to conclude whether or not the results

observed are a consequence of the effects of the oil or ifthey fall within the range of ecosystem variability. There-fore long data series are essential to make an assessmentof any anthropogenic impact. In the present study the datasupplied by the IEO Core Project, Studies on time Series of

Oceanographic Data, provided sound information on thenatural variability of the pelagic ecosystem at different lev-els of the planktonic component, allowing for a realisticevaluation of oil effects.

The results of this study have showed, on the one hand,the great natural variability of the pelagic ecosystem of theN–NW Spanish coast, and on the other, the lack of detect-able effects of Prestige oil on planktonic communities.However we cannot ascertain whether or not there are, infact, effects. In this ecosystem, influenced by large andmeso-scale hydrological phenomena as well as a markedseasonality in the development of biological processes,the great variability of planktonic cycles will probably con-ceal any low intensity effect.

In our case it is unlikely that Prestige shipwreck had anyrelevant effect even in the short-term. Not only were theconcentrations of oil measured during the study periodlow, but also the fuel observed was not always related tothe wreck (Gonzalez et al., this issue). The few significantchanges observed in phytoplankton species compositionand zooplankton biomass may be explained by changesin environmental conditions over the course of the year2003. The phytoplankton species showing significantlyhigher values in spring (Table 1), are typical of upwellingconditions, which are predominant during the summer inthis area (Casas et al., 1999). Upwelling events started ear-lier in 2003—in March and April in the Galician andSouthern Bay of Biscay (Ruiz-Villareal et al., this issue).This advance in the upwelling season could explain thehigher biomass of these phytoplankton species. The higherzooplankton biomass found occasionally in summermonths (Figs. 6–8) may be related to the unusually warmtemperatures during the summer of 2003. These tempera-tures coincided with reduced upwelling intensity (Ruiz-Vil-lareal et al., this issue), but it was still strong enough tomaintain relatively high values of chlorophyll (Figs. 2and 3) to support an large zooplankton biomass withincreasing growth rates favoured by warmer waters. There-fore, the few variations found in plankton may beexplained by natural changes in the environmental condi-tions of the ecosystem of the area of study and not byeffects caused by the Prestige oil spill.

5. Conclusions

No relevant effects on the pelagic system were observedin the study area. There were not any noticeable changes inphytoplankton primary production and no alterations ineither phytoplankton or zooplankton biomass weredetected as compared to previous years. The phytoplank-ton and zooplankton community structure did not exhibitany significant differences before and after the spill. Despite

284 M. Varela et al. / Marine Pollution Bulletin 53 (2006) 272–286

the fact that zooplankton copepods were found to be con-taminated with oil—externally as well as internally—noharmful effects were observed to cause changes in the bio-mass or community structure.

Only a few, occasional variations were observed inplankton communities, but they were related to variationson a temporal scale of oceanographic processes typical ofthis ecosystem, mainly upwelling of ENACW, and not tothe effect of the oil.

Through field studies, we are unable to ascertainwhether or not oil has affected plankton, especially in theshort-term, because meso and large-scale hydrographicprocesses can cause extreme variability in plankton, mask-ing any effect of the oil, especially when, as in this case, theeffect is reduced or short-lived.

In the case of new spills, the studies of the effects onplankton must be extended until the next important biolog-ical period, such as, in our case, the phytoplankton springbloom, with special emphasis on plankton communitystructure. In areas where the probability of oil spills is highand no previous information exists, monitoring programsshould be implemented to obtain information on theyear-to-year variability of the ecosystem.

Acknowledgements

We are extremely grateful to the crews of RV Navaz,Lura and Rioja from the IEO for their help and assistanceduring the sampling. The study was carried out within theframework of the IEO Core project Studies on Time Seriesof Oceanographic Data. We would also like to thank theperson responsible for the EU projects Pelasses and Sardyn

for allowing our participation in the Pelacus cruises inspring in the continental shelf area of N–NW Spain.

We are indebted to the many technicians participating inthe sampling and to the Directors of the IEO Coastal Cen-tres for allowing us unrestricted use of the laboratory facil-ities, without which facilitating the sampling andprocessing of samples would not have been possible.

This paper is a contribution to the Strategic Action ofthe Spanish Ministry of Science and Technology, imple-mented to study the influence of the Prestige oil spill onthe pelagic system during the spring period following theshipwreck. C. Garcıa-Soto would like to acknowledge aRamon y Cajal contract and financial support from theproject VEM 2004-08613. This work was partially fundedby the Natural Environment Research Council core sup-port of Plymouth Marine Laboratory.

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